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Journal of Environmental and Occupational Science www.jenvos.com Original Research DOI: 10.5455/jeos.20170120094512 A study of airborne fungal allergens in sandstorm dust in Al-Zuli, central region of Saudi Arabia Rajendran Vijayakumar1, Mohammad Saleh Al-Aboody1, Wael Alturaiki1, Suliman A. Alsagaby1, Tim Sandle2 1 Department of Medical Laboratories, Central Biosciences Research Laboratories, College of Science in Al-Zulfi, Majmaah University, Al Majmaah, Kingdom of Saudi Arabia, 2Department of Microbiology, Bio Products Laboratory, Elstree, Hertfordshire, United Kingdom Address for correspondence: Rajendran Vijayakumar, Department of Medical Laboratories, Central Biosciences Research Laboratories, College of Science in Al-Zulfi, Majmaah University, Kingdom of Saudi Arabia. E-mail: v.kumar@ mu.edu.sa Received: December 03, 2016 Accepted: December 21, 2016 Published: April 09, 2017 ABSTRACT Background: The impact of sandstorm dust events on local air quality and public health are becoming a greater concern in the Kingdom of Saudi Arabia. Among sandstorm dust particles, airborne fungal spores cause serious respiratory ailments to those who are exposed to the dust. Although the study of dust storm material has attracted research interest, little work has been carried out in Saudi Arabia and no major study has been conducted in the Al-Zulfi, Riyadh province region. Hence, the aim of the study was to investigate airborne fungal allergen concentrations in sandstorm dust in the Al-Zulfi city, Saudi Arabia. Materials and Methods: During the study period, 12 sandstorm dust samples and 3 control samples were collected from various locations (educational campus, people gathering, and recreational places) by gravitational plate exposure method using Sabouraud dextrose agar. Following incubation, the fungal colonies were identified by microscopic and morphological identification. Results: A total of 2590 fungal isolates were identified among 36 exposures of sandstorm dust samples. From the samples dematiaceous fungi and hyaline fungi were observed, divided 56.2%, 43.8%, respectively. The incidences of predominant fungal genera were Fusarium (21%), Cladosporium (15.8%), Ulocladium (11.1%), Aspergillus (10.9%), and Alternaria (8.6%). Conclusion: Our observations infer that some of the most important allergenic fungal spores are predominantly observed in sandstorm dust samples and incidences of dematiaceous fungi are higher than hyaline fungi. This study highlights the need for precautionary safety measures to protect the public against sandstorm dust exposures. KEY WORDS: Alternaria, air sampling, Cladosporium, dust, fungal allergens, Fusarium, sandstorm, settle plate INTRODUCTION Sandstorms, also called dust storms, occur frequently and periodically under the strong winds which blow dust across the dry deserts around the globe, especially in the Middle East. The Kingdom of Saudi Arabia (KSA) is the largest country in the region and it constitutes the vast majority of the Arabian Peninsula. Most the land surface is made up of deserts and semiarid lands. Based on its topography and condition of drought, light textured topsoil, and scanty vegetative cover much of the region and thus the KSA is highly susceptible to sandstorm dust. Sandstorm episodes in the deserts of KSA are seasonal, with the majority of atmospheric transport occurring within the February to May months [1]. Notwithstanding this seasonal pattern, a significant increase in frequency and the intensity of sand and dust storms has been observed in the Middle East over the past 15 years [2]. In addition to the KSA and Middle East countries, all sandstorms facilitate the long-distance dispersal J Environ Occup Sci ● 2017 ● Vol 6 ● Issue 1 of dust-associated biological particles includes bacteria, fungi, and viruses, and it is not uncommon for these organisms to be carried across several continents [3]. According to the WHO, dust storms contribute to poor air quality and this is attributed to the death of around 7 million people every year [4]. A proportion of these deaths will relate to fungi; there are several thousand of types of fungal spores found in both indoor and outdoor environments including sand dust; moreover, as well as species diversity, a significantly high number (around 106) of spores are found in sandstorm dust [1,5]. The medical risk to human health arises from the fungi associated with sandstorm dust producing metabolites (mycotoxins) that can initiate a toxic response to humans. Here repeated exposure causes respiratory irritation or allergic sensitization [1,6]. Inhalation exposure of fungal spore and hyphal fragments can cause allergic, infectious, and toxic diseases to humans. Infants, children, and elderly people with 27 Vijayakumar, et al.: Airborne fungal allergens in sandstorm dust respiratory conditions are more vulnerable compared with the general population [7,8]. Prolonged exposure to airborne dust fungi can lead to chronic breathing and lung problems, and possibly heart disease. As medical understanding advances, the impact of severe sandstorm dust events on local air quality and public health have become of greater concern in the KSA in recent years. Although the study of dust storm material has attracted many researchers globally, little work has been undertaken in the KSA [7,9]. Furthermore, there has been no published work performed in relation to the central region of the Arabian Desert. Hence, the aim of this work was to isolate fungal allergens in sandstorm dust and analyze the incidence of allergens in the central region of KSA. MATERIALS AND METHODS Study Site Al-Zulfi is a city in Riyadh province in the central desert region of the KSA, about 260 kilometers northwest of Riyadh. Al-Zulfi lies in the northern-central region of the Najd and to the south of the Samnan Valley. The city surrounded by sand dunes to its north and west, which are known locally as the Al-Thoyr Sands. This study was conducted at the various places of Al-Zulfi, including the educational campus (College of Science, AlZulfi), an area with a high population density (Zulfi Dates market) and a recreational place (Zulfi West – City view). Samples were taken during sandstorms and during periods when no sandstorms were occurring. based on macroscopic and microscopic morphology following the keys and description given by Samson et al., Lalitha et al., and Vijayakumar et al., [13-15]. To compare the fungal counts with a non-sandstorm episode (to act as a control), the same procedure was followed and samples collected for one period under non-sandstorm conditions. The significance of the incidences of fungal allergens, among the various sampling locations, was analyzed using Student’s t-test, a P < 0.05 was considered as statistically significant. RESULTS During the study period, 12 sandstorm dust sample sets were collected. These consisted of six sets from the educational campus; three sets from the people gathering area (Zulfi dates market); three sets from Zulfi city – west view location [Figure 1]. Triplicate samples were taken for each sample set and a total of 2590 fungal colonies were observed from the 36 exposed plates. In addition, from the educational campus during non-sandstorm conditions a total 3 samples (9 exposures) were collected (during the daytime). All samples taken are listed in Table 1. The total fungal colonies observed from the educational campus ranged from 12 to 87 CFU/plate. In the people gathering area significantly higher levels of fungi were recorded compared with the educational campus (P = 0.032). With the three sets (9 exposures) performed in the Zulfi dates market area, all samples were collected during busy periods such as 4-6 pm. With these samples, the range of mold colonies was 87-131 CFU/plate. A further 9 exposures were performed in the Zulfi city west view Sampling Methods Sampling was undertaken by a passive air sampling method (settle plates, where fungal spores are capture by gravitational deposition). This was performed using agar-filled Petri dishes exposed at a 1-m height from the surface [10]. Each Petri dish contained (90 mm diameter) Sabouraud dextrose agar (SDA) (sometimes described as Sabouraud glucose agar) (Himedia, India). SDA is an agar especially formulated, through the inclusion of peptones, for the isolation and growth of dermatophytes and other types of fungi [11]. A total of 12 sandstorm episodes occurred during the study period, from the beginning of February 2016 to the end of May 2016. During each sandstorm, one of the identified locales was sampled and for each sampling location triplicate SDA plates were exposed (in total 36 samples were taken across the course of the study). The metrological parameters such as temperature and wind speed were recorded (obtained from an internet source) [12]. After sampling, the plates were incubated at 20-25°C for 6-8 days. The total fungal colonies were counted and recorded on the 2nd or 3rd day of incubation, and then, at the end of incubation. For further species identification, fungal colonies were subcultured to a second SDA plate and then incubated for 5-7 days. Fungal identification performed 28 a b Figure 1: The impact of sandstorm over the Al-Zuli city, (a) Clear atmospheric condition on March 22, 2016, and (b) sandstorm episode on March 27, 2016 J Environ Occup Sci ● 2017 ● Vol 6 ● Issue 1 Vijayakumar, et al.: Airborne fungal allergens in sandstorm dust area and these showed a range of 34-110 CFU/plate. Control samples (9 exposures) were collected from the next day after a sandstorm had occurred (that is non-sandstorm conditions with an observable clear sky); here all plates showed less than 15 CFU/plate [Table 1]. The total of 2590 fungi isolated from the 36 exposures of sandstorm dust samples is listed in Table 2. Based on a microscopic and macroscopic morphological identification of the fungi, 13 different genera of fungi were identified from the isolates. The predominant colonies were species of Fusarium (21%) followed by Cladosporium, Ulocladium, Aspergillus, Alternaria, and Penicillium (15.8%, 11.1%, 10.9%, 8.6%, and 7.3%, respectively). The totality of dematiaceous fungi isolated (56.2%) was greater than hyaline fungi (43.8%) (P < 0.0001). A proportion of the fungi (9.3%) could not be identified due to a lack of sporulation. These have been reported as “unidentified dematiaceous” and “hyaline fungi,” respectively. The ranking of incidence of fungi and their pathogenicity to cause allergic diseases (based on comparable with worldwide reports) are listed in Table 3. DISCUSSION A significant increase in the frequency and the intensity of sand and dust storms has been observed in the Middle East Table 1: Total number of fungal colonies observed from the exposed sandstorm dust samples Sample ID Description Temperature/Wind Number of fungal colonies (CFU/plate) S1 Sandstorm samples SS 1 SS 2 SS 3 SS 4 SS 5 SS 6 SS 7 SS 8 SS 9 SS 10 SS 11 SS 12 Control samples (non‑sandstorm) NS 1 NS 2 NS 3 S2 S3 Arithmetic mean Geometric mean Educational campus Educational campus Educational campus Educational campus Educational campus Educational campus Zulfi Dates Market Zulfi Dates Market Zulfi Dates Market Zulfi – City view (East) Zulfi – City view (East) Zulfi – City view (East) 38°C; 42 km/h 35°C; 35 km/h 31°C; 28 km/h 35°C; 19 km/h 30°C; 31 km/h 37°C; 28 km/h 27°C, 40 km/h 28°C, 8 km/h 31°C; 22 km/h 38°C; 42 km/h 30°C; 32 km/h 32°C; 28 km/h 76 27 36 12 62 82 107 116 87 91 110 34 83 48 39 21 74 69 121 128 95 94 88 38 56 32 28 28 87 76 115 131 96 67 96 40 71.67 35.67 34.33 20.33 74.33 75.67 114.33 125.00 92.67 84.00 98.00 37.33 70.69 34.61 34.00 19.18 73.63 75.48 114.19 124.83 92.58 83.06 97.58 37.25 Educational campus Zulfi Dates Market Zulfi – City view (East) 33°C; 12 km/h 35°C; 10 km/h 34°C; 13 km/h 2 6 6 4 8 12 3 11 14 3.00 8.33 10.67 2.88 8.08 10.03 Total 2590 215 107 103 61 223 227 343 375 278 252 294 112 66 9 25 32 S1: Exposed plate 1, S2: Exposed plate 2, S3: Exposed plate 3 Table 2: Total number and distribution of molds from the each sample Name of the organism SS 1 SS 2 SS 3 SS 4 SS 5 SS 6 SS 7 SS 8 SS 9 SS 10 SS 11 SS 12 Total (%) 35 17 19 8 19 8 12 118 16 8 10 3 10 4 7 58 16 7 10 4 7 3 8 55 10 3 7 2 6 3 4 35 34 15 20 7 25 11 14 126 37 12 21 9 28 9 13 129 52 31 30 12 41 14 15 195 65 27 31 14 40 15 20 212 40 18 24 11 31 11 21 156 39 16 19 10 28 11 17 140 47 16 24 12 39 11 18 167 18 7 9 4 14 4 8 64 409 (15.8) 177 (6.8) 224 (8.6) 96 (3.7) 288 (11.1) 104 (4.0) 157 (6.1) 1455 (56.2) 47 8 6 4 4 15 1 0 1 1 10 97 215 24 4 3 2 2 7 0 0 1 0 6 49 107 21 6 3 2 1 9 0 1 0 0 5 48 103 15 2 2 1 0 5 0 0 0 0 1 26 61 47 9 7 6 4 16 1 1 1 1 4 97 223 50 7 7 3 3 17 0 1 1 1 8 98 227 61 15 14 7 7 25 2 1 1 2 13 148 343 80 16 12 8 6 27 2 2 2 1 7 163 375 60 11 9 6 5 20 1 0 1 1 8 122 278 51 9 8 6 4 18 2 1 1 1 11 112 252 63 12 9 5 6 21 2 0 2 1 6 127 294 24 4 3 2 1 8 0 0 1 0 5 48 112 543 (21.0) 103 (4.0) 83 (3.2) 52 (2.0) 43 (1.7) 188 (7.3) 11 (0.4) 7 (0.3) 12 (0.5) 9 (0.3) 84 (3.2) 1135 (43.8) 2590 (100) Dematiaceous fungi Cladosporium spp. Curvularia spp. Alternaria spp. Bipolaris spp. Ulocladium spp. Exserohilum spp. UIDF Total ‑Dematiaceous fungi Hyaline fungi Fusarium spp. Aspergillus niger Aspergillus flavus Aspergillus fumigatus Aspergillus spp. Penicillium spp. Scedosporium spp. Mucor spp. Rhizopus spp. Paecilomyces spp. UIHF Total – hyaline fungi Grand total UIDF: Unidentified dematiaceous fungi, UIHF: Unidentified hyaline fungi J Environ Occup Sci ● 2017 ● Vol 6 ● Issue 1 29 Vijayakumar, et al.: Airborne fungal allergens in sandstorm dust Table 3: Incidence of commonly occurring fungal genera in this study and comparable with worldwide available reports Rank Fungal genera (Percentage of incidence in this study) Predominantly reported in dust source region (References) Reported pathogenicity to allergies I II Fusarium (21%) Cladosporium (15.8%) Allergen related disease Potent allergen related disease III IV Ulocladium (11.1%) Aspergillus (10.9%) Turkey [30], Taiwan [35] Saudi Arabia [8], Egypt [29], Turkey [30], Iran [31], Taiwan [35], Africa [37] Saudi Arabia [8], Taiwan [35] Saudi Arabia [8,9], Taiwan [36], Africa [37], Mali [38], Mid Atlantic [39], Israel [40] V Alternaria (8.6%) VI Penicillium (7.3%) VII Curvularia (6.8%) Saudi Arabia [8], Turkey [30], Taiwan [36], Africa [37], Mali [38], Mid Atlantic [39], Israel [40] Saudi Arabia [8], Turkey [30], Taiwan [36], Mid Atlantic [39] Taiwan [35] No reports Aspergillosis (Pulmonary allergic and colonizing), Number of different allergen related diseases in the immunocompromised person Potent allergen (common causative agent of extrinsic asthma) Potent allergen related disease Allergen‑related disease over the past 15 years. Although the focal point has been the Middle East, with Iran and Kuwait the most affected, meteorologists have recorded similar step-changes in activity in some parts of Central Asia [2]. This global rise in incidences makes the study of fungal spores in the generated dust a subject of medical importance. Human health is adversely affected by the exposure of sandstorm dust because the dust carries numerous pollutants such as allergens and microorganisms that can affect human health. Hence, there is the need for detailed studies about the microorganisms distributed the sandstorm dust, particularly fungi capable of causing allergic diseases. In the people gathering area (market), this locale showed higher recoveries than with the educational campus (P = 0.0079). With the market area, three sample sets (9 exposures) were collected. Each of the samples was collected during busy periods (4-6 pm) and the range of mold colonies was between 87 and 131 CFU/plate. These sampling sites will be affected by the density of people and their increased activities. The numbers of fungi recovered will be influenced by the people, for humans continually shed microorganisms (including fungi) from the outer surface of the skin [17], and this may account for the increased number of fungal counts compared with the other areas sampled. Each geographical area will vary in the range and types of microorganisms recovered. Overall, there are very few research articles available about fungal genera in sandstorm dust environment and there have been none reported relating to the central region of the KSA. The location selected for study was important in terms of geography. Al-Zulfi city lies in the northern-central region of the Najd and to the south of the Samnan Valley of Saudi Arabia. It is surrounded by sand hills to its north and west and consequently Al-Zulfi city is subject to regular sandstorms because of the city surrounded by sand hills. In this study, species of Fusarium (21%), Cladosporium (15.8%), Ulocladium (11.1%), Aspergillus (10.9%), Alternaria (8.6%), and Penicillium (7.3%) are predominantly present in all of the sandstorm dust samples. This is similar to another study conducted in the KSA by Kwassi and his coworkers, which reported that the most abundant fungal genera in sandstorm dust were Alternaria, Aspergillus, and Cladosporium [8]. These predominant genera were comparable with other research reports relating to the Middle East countries of Kuwait and Qatar [18,19]. For example, the most prevalent fungal genera in airborne dust samples collected from the atmosphere of Taif, KSA, were (31 genera and 70 species) Aspergillus, Drechslera, Fusarium, Mucor, Penicillium, Phoma, and Stachybotrys [20]. In a large series study carried out by Abu Dieyeh and his coworkers in Zarqa desert region, Jordan, this reported that the highest abundance of fungi were attributable to Cladosporium (29.1%) followed by Fusarium (20%), Alternaria (7.7%), Ulocladium (6.5%), Penicillium (4.2%), and Aspergillus (3.6%) [21]. With this study, 36 exposures of sandstorm dust samples were collected in three different environments (an educational campus, a people gathering area, and a recreational place). These were compared to control (non-sandstorm) samples. The total numbers of fungal colonies observed from the exposed plates was 2590. Across the three locations, the numbers of fungi were higher compared with the control, indicating that airborne fungal populations are significantly elevated during sandstorms (between 3 and 10-fold higher; P = 0.0066). In relation to metrological factors many researchers have reported that weather patterns cause significant effects on the concentration of airborne fungal spores [1,16]; in this study, all samples collected under conditions that were metrologically assessed and it was noted that the wind velocity was >20 km/h during each sandstorm episode. This fact alone appears to yield more fungal airborne particles compared with the periods when the control samples were collected. 30 While the genera were generally similar, our study showed a higher proportion of species of Fusarium. This may be reflective of a niche environment since incidences of fungal genera will vary among regions based on the “true” microbial community, or it could be a product of the sampling method, agar selected, incubation time, and identification methods. For example, the most well-known human pathogens associated with desert dust storms and dust exposure originating from dried bird faces are Coccidioides immitis and Histoplasma capsulatum, respectively, yet these have been found only in the J Environ Occup Sci ● 2017 ● Vol 6 ● Issue 1 Vijayakumar, et al.: Airborne fungal allergens in sandstorm dust Americas [22,23] and none of these pathogens were reported in this study’s findings. This reaffirms that desert environments harbor diverse mycological communities and with this there are regional variations. Another interesting finding relates to the incidence of dematiaceous fungi from the sandstorm dust, which was slightly higher (at 56.2%) compared to hyaline fungi (43.8%). This ratio is similar to another report [18]. The ratio is significant since the dematiaceous fungi cell wall contains a melanin pigment that contributes to the virulence of pathogens of humans as well as those of food crops. In addition, the pigment enhances fungal resistance to environmental damage. Several authors have reported that dematiaceous fungal spores are highly prevalent in hot climate atmospheres and they are more resistant to desiccation [24] and ultraviolet radiation [25], compared with hyaline fungi. With individual predominant fungal genera, Fusarium was the most predominant species in this study with the total contribution of 21%. Notably, the Jordan study reported that Fusarium species are found at a high incidence during the month of May [21]. Given that our study’s sampling duration covered the month of May, this could be the reason for the high percentage recovery of this fungus. A further reason for the prevalence relates to Fusarium being a well-known plant pathogen and one that is frequently isolated from the soil. Because sandstorm wind speeds, recorded in our study were typically between 30 and 40 km/h, the wind will carry sand dust materials from the agricultural surroundings of the city and this may contribute to the high incidence of Fusarium species in the atmosphere. Similarly, Fusarium species were reported as the most abundant species in the atmosphere with the Tel-Aviv, Israel study [26]. Cladosporium species was the second most predominant species in our study findings, and this is similar to several aeromycological studies from around the world [16,18,21,27,28]. Many reports from the countries nearby the KSA such as Jordan [21], Qatar [18], Egypt [29], Turkey [30], and Iran [31] have reported Cladosporium as the most predominant dematiaceous fungi. This coincides with our research which showed that at a percentage of 15.8%, Cladosporium are frequently isolated from the air and soil. Many authors have reported that the high percentage of Cladosporium may be attributed by the size of spores and smooth wall which favor and facilitate the transport of airborne spores in sandstorms. A further factor favoring this fungus is due to the spores being highly resistant to hot climates [18,32]. Another predominant dematiaceous airborne fungus is Alternaria species. With our study, the incidence of this fungus was 8.6%. Species of Alternaria are commonly reported as predominant fungal contaminants from outdoor environments [33]. A large sandstorm study conducted by Kwaasi et al., (1998) at Riyadh, Saudi Arabia reported that the predominant fungal genera were Alternaria, Aspergillus, and Cladosporium [8]. These findings reaffirm what this study reports. J Environ Occup Sci ● 2017 ● Vol 6 ● Issue 1 According to the available reports from the various desert regions worldwide, the fungal genera of Aspergillus, Alternaria, Cladosporium, Curvularia, Fusarium, and Penicillium isolated from the sandstorm dust sources are mild to potent allergens [1,34-40]. During dust storms, a variety of airborne microbial particles remain suspended in the fine dust and some get blown over long distances and they can be forcibly introduced into human orifices such as eyes, nostrils, and ears [1,4,34]. Those particles which are <10 µm in size can penetrate into the lungs and those of <2.5 µm can penetrate into the subepithelial environment and can cause an allergic response. The spore sizes of the predominant fungal general reported in this study are less than 10 µm and thus they could cause an allergic reaction. In addition, this study has indicated that some of the most important allergenic fungal spores were isolated from the sandstorm dust in high numbers. These were Alternaria, Aspergillus, Cladosporium, Curvularia, Fusarium, Paecilomyces, and Penicillium. Thus, based on size and morphology, the fungi contained in sandstorm dust can potentially cause allergenic respiratory problems with those who are exposed to sandstorm dust. These tallies with a recent study from the KSA, which reported that people exposed to a sandstorm for duration of 24 min developed various respiratory complaints including asthma [7]. The report from KSA reaffirms that sandstorms carry numerous allergens through the air and with 70% of Saudi Arabian asthmatics already suffering from allergies, the risk of respiratory complications due to sandstorms is extremely high. In one single sandstorm in 2015 over 400 Saudi Arabian citizens were hospitalized due to respiratory problems, of this one quarter of the admissions was pediatric [34]. Based on the findings of this study that sandstorm dust carries fungal spores which cause an allergenic response in humans, we recommend that precautionary measures be taken to minimize exposure to the sandstorm dust. In particular, preventative recommendations should be made to outside workers and for returning residents. Such measures should be based on the use of appropriate personal protective equipment (dust mask) as well as avoiding unnecessary exposure to the dust. Various types of facemasks available to the general public can protect against inhalation of dust, pollutants, allergens, and pathogenic organisms. In addition, airtight goggles can be worn. It is important for children with chronic respiratory problems to avoid all outdoor activity during a sandstorm. Another important recommendation is for people who wear contact lenses. Here contact lens wearers should not expose their contact lenses to dust and people should ideally wear eyeglasses (or goggles) during a sandstorm. Where contact lenses are worn these should always be kept clean otherwise the dust exposure may lead to a corneal ulcer developing. Limitations of the Study The main limitation of the study was with the control samples. These were collected for only one sample (3 exposures) per location. This was because the control samples were used only for comparisons and the main aim of the work was to analyze 31 Vijayakumar, et al.: Airborne fungal allergens in sandstorm dust the fungal allergens in sandstorm dust samples. A baseline for non-sandstorm conditions can be developed through further study. 11. CONCLUSION 12. This study concludes that sandstorm dust from the central region of the KSA carries high numbers of fungal spores. The predominant fungal spores are Fusarium, Cladosporium, Ulocladium, Aspergillus, and Alternaria. The concentrations of these fungi are high as compared with non-sandstorm periods. Of the different types of fungi, dematiaceous fungi incidences are higher than hyaline fungi. The predominant fungal spores characterized can act as potent allergens and cause respiratory allergic diseases. To the best of our knowledge, this study is the first to highlight the distribution of fungal genera in sandstorm dust from the Al-Zulfi region, the central region of KSA. This study recommends that protective measures such as wearing a mask to minimize the respiratory asthmatic diseases and airtight goggles to protect the eyes. Finally, further studies of aeromycological levels are needed to further understand the microbial ecology, biogeography, and spread of fungal allergens in sandstorm dust. 13. 14. 15. 16. 17. 18. 19. 20. 21. ACKNOWLEDGMENT This research work was funded by the Basic Science Research Unit, Deanship of Scientific Research at Majmaah University, KSA (Year 1436-37). REFERENCES 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 32 Griffin DW. Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin Microbiol Rev 2007;20:459-77. Significant increase in frequency and intensity of sandstorms in the Middle East over the past 15 years, The Watchers; 2016. Available from: https://www.watchers.news/2016/06/17/significant-increasein-frequency-and-intensity-of-sandstorms-in-the-middle-east-overthe-past-15-years/. [Last accessed on 2016 Nov 16]. Goudie AS, Middleton NJ. Saharan dust storms: Nature and consequences. Earth Sci Rev 2001;56:179-204. World Health Organization. Global Surveillance, Prevention and Control of Chronic Respiratory Disease; A Comprehensive Approach; 2007. Available from: http://www.who.int/gard/publications/ GARD%20Book%202007. [Last accessed on 2016 Nov 16]. Prospero JM, Blades E, Mathison G, Naidu R. Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia 2005;21:1-19. Robbins CA, Swenson LJ, Nealley ML, Gots RE, Kelman BJ. Health effects of mycotoxins in indoor air: A critical review. Appl Occup Environ Hyg 2000;15:773-84. Meo SA, Al-Kheraiji MF, Alfaraj ZF, Alwehaibi NA, Aldereihim AA. Respiratory and general health complaints in subjects exposed to sandstorm at Riyadh, Saudi Arabia. Pak J Med Sci 2013;29:642-6. Kwaasi AA, Parhar RS, Al-Mohanna FA, Harfi HA, Collison KS, AlSedairy ST. Aeroallergens and viable microbes in sandstorm dust. Potential triggers of allergic and nonallergic respiratory ailments. Allergy 1998;53:255-65. Al-Barakah F, Radwan SM, Modaihsh AS. Seasonal and spatial variation of microbial contents in falling dusy in Riyadh city, Saudi Arabia. Int J Curr Microbiol Appl Sci 2014;3:647-56. Buttner MP, Stetzenbach LD. Monitoring airborne fungal spores in an experimental indoor environment to evaluate sampling methods and 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. the effects of human activity on air sampling. Appl Environ Microbiol 1993;59:219-26. Gebala B, Sandle T. Comparison of different fungal agar for the environmental monitoring of pharmaceutical-grade cleanrooms. PDA J Pharm Sci Technol 2013;67:621-33. The Weather Channel, Al-Zulfi, Saudi Arabia; 2016. Available from: https://www.weather.com/weather/today/1/26.31,44.83. [Last accessed on 2015 May 15]. Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O. Introduction to Food-and Airborne Fungi. Utrecht: Centraal Bureau Voor Schimmel Cultures; 2002. Lalitha P, Vijayakumar R, Prajna NV, Srinivasan M. Atlas of Fungal Corneal Ulcer – Clinical Features & Laboratory Identification Methods. India: Jaypee Publishers; 2008. Vijayakumar R, Sandle T. Manoharan C. A review of fungal contamination in pharmaceutical products and phenotypic identification of contaminants by conventional methods. Eur J Parent Pharm Sci 2012;17:4-19. Asan A, Ilhan S, Sen B, Erkara I, Filik C, Cabuk A, et al. Airborne fungi and actinomycetes concentrations in the air of Eskisehir City (Turkey). Indoor Built Environ 2004;13:63-74. Sandle T. From head to toe: Mapping fungi across human skin. EC Microbiol 2015;2:211-3. Al-Subai AA. Air-borne fungi at Doha, Qatar. Aerobiologia 2002;18:175-83. Moustafa AF, Kamel SM. A study of fungal spore poupulations in the atmosphere of Kuwait. Mycopathologia 1976;59:29-35. Abdel-Hafez SI, Shoreit AA. Mycotoxins producing fungi and mycoflora of air-dust from Taif, Saudi Arabia. Mycopathologia 1985;92:65-71. Abu-Dieyeh MH, Barham R, Abu-Elteen K, Al-Rashidi R, Shaheen I. Seasonal variation of fungal spore populations in the atmosphere of Zarqa Area, Jordan. Aerobiologia 2010;26:263-76. Hector RF, Laniado-Laborin R. Coccidioidomycosis - A fungal disease of the Americas. PLoS Med 2005;2:e2. Morgan J, Cano MV, Feikin DR, Phelan M, Monroy OV, Morales PK, et al. A large outbreak of histoplasmosis among American travelers associated with a hotel in Acapulco, Mexico, spring 2001. Am J Trop Med Hyg 2003;69:663-9. Rosa LH, Almeida Vieira Mde L, Santiago IF, Rosa CA. Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol Ecol 2010;73:178-89. Tolleson WH. Human melanocyte biology, toxicology, and pathology. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2005;23:105-61. Kessler A. Survey of airborne pollen and mold spores in Israel, 19541955. Ann Allergy 1958;16:445-50. Ismail MA, Abdel-Hafez SI, Moharram AM. Aeromycobiota of western desert of Egypt. Afr J Sci Technol 2002;3:1-9. Nourian AA, Badali H, Khodaverdi M, Hamzehei H, Mohseni S. Airborne mycoflora of Zanjan-Iran. Int J Agric Biol 2007;9:628-30. Awad AH, Gibbs SG, Tarwater PM, Green CF. Coarse and fine culturable fungal air concentrations in urban and rural homes in Egypt. Int J Environ Res Public Health 2013;10:936-49. Griffin DW, Kubilay N, Kocak M, Gray MA, Borden TC, Kellogg CA, et al. Airborne desert dust and aeromicrobiology over the Turkish Mediterranean coastline. Atmos Environ 2007;41:4050-62. Nourmoradi H, Moradnejadi K, Moghadam FM, Khosravi B, Hemati L, Khoshniyat R, et al. The effect of dust storm on the microbial quality of ambient air in Sanandaj: A city located in the west of Iran. Glob J Health Sci 2015;7:114-9. El-Morsy ES. Preliminary survey of indoor and outdoor airborne microfungi at coastal buildings in Egypt. Aerobiologia 2006;22:197-210. Al-Qurashi AM. Profiles of airborne fungi in schools of Saudi Arabia in relation to the allergy problems and respiratory diseases. J Food Agric Environ 2007;5:69-73. Tawalbeh K, Al-Jassem D. Dust Forces residents to stay indoors. Arab News 2012. Available from: http://www.arabnews.com/node/409061. [Last accessed on 2016 Nov 16]. Ho HM, Rao CY, Hsu HH, Chiu YH, Liu CM, Chao HJ. Characteristics and determinants of ambient fungal spores in Hualien, Taiwan. Atmos Environ 2005;39:5839-50. J Environ Occup Sci ● 2017 ● Vol 6 ● Issue 1 Vijayakumar, et al.: Airborne fungal allergens in sandstorm dust 36. 37. 38. 39. Wu PC, Tsai JC, Li FC, Lung SC, Su HJ. Increased levels of ambient fungal spores in Taiwan are associated with dust events from China. Atmos Environ 2004;38:4879-86. Griffin DW, Kellogg CA, Garrison VH, Lisle JT, Borden TC, Shinn EA. Atmospheric microbiology in the northern Caribbean during African dust events. Aerobiologia 2003;19:143-57. Kellogg CA, Griffin DW, Garrison VH, Peak KK, Royall N, Smith RR, et al. Characterization of aerosolized bacteria and fungi from desert dust events in Mali, West Africa. Aerobiologia 2004;20:99-110. Griffin DW, Westphal DL, Gray MA. Airborne microorganisms in the African desert dust corridor over the mid-Atlantic ridge, Ocean Drilling Program, Leg 209. Aerobiologia 2006;22:211-26. J Environ Occup Sci ● 2017 ● Vol 6 ● Issue 1 40. Schlesinger P, Mamane Y, Grishkan I. Transport of microorganisms to Israel during Saharan dust events. Aerobiologia 2006;22:259-73. © eJManager. This is an open access article licensed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted, noncommercial use, distribution and reproduction in any medium, provided the work is properly cited. Source of Support: Nil, Conlict of Interest: None declared. 33